Muscle catabolic capacities and global hepatic epigenome are modified in juvenile rainbow trout fed different vitamin levels at first feeding

Abstract

Based on the concept of nutritional programming in mammals, we tested whether a short term hyper or hypo vitamin stimulus during first-feeding could induce long-lasting changes in nutrient metabolism in rainbow trout. Trout alevins received during the 4 first weeks of exogenous feeding a diet either without supplemental vitamins (NOSUP), a diet supplemented with a vitamin premix to satisfy the minimal requirement in all the vitamins (NRC) or a diet with a vitamin premix corresponding to an optimal vitamin nutrition (OVN). Following a common rearing period on the control diet, all three groups were then evaluated in terms of metabolic marker gene expressions at the end of the feeding period (day 119). Whereas no gene modifications for proteins involved in energy and lipid metabolism were observed in whole alevins (short-term effect), some of these genes showed a long-term molecular adaptation in the muscle of juveniles (long-term effect). Indeed, muscle of juveniles subjected at an early feeding of the OVN diet displayed up-regulated expression of markers of lipid catabolism (3-hydroxyacyl-CoA dehydrogenase – HOAD - enzyme) and mitochondrial energy metabolism (Citrate synthase - cs, Ubiquitinol cytochrome c reductase core protein 2 - QCR2, cytochrome oxidase 4 - COX4, ATP synthase form 5 - ATP5A) compared to fish fed the NOSUP diet. Moreover, some key enzymes involved in glucose catabolism (Muscle Pyruvate kinase - PKM) and amino acid catabolism (Glutamate dehydrogenase - GDH3) were also up regulated in muscle of juvenile fish fed with the OVN diet at first-feeding compared to fish fed the NOSUP diet. We researched if these permanently modified gene expressions could be related to global modifications of epigenetic marks (global DNA methylation and global histone acetylation and methylation). There was no variation of the epigenetic marks in muscle. However, we found changes in hepatic DNA methylation, global H3 acetylation and H3K4 methylation, dependent on the vitamin intake at early life. In summary, our data show, for the first time in fish, that a short-term vitamin-stimulus during early life may durably influence muscle energy and lipid metabolism as well as some hepatic epigenetic marks in rainbow trout. Statement of relevanceProgramming at first feeding with different levels of vitamins was successfully tested in fish for the first time. These data proove one more time the importance of the early life on the fish metabolism in adults.